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Effects of Seed Beetles on the Performance of Desert Legumes Depend on Host Species, Plant Stage, and Beetle Density

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Effects of Seed Beetles on the Performance of Desert Legumes Depend on Host Species, Plant Stage, and Beetle Density Journal of Arid Environments 80 (2012) 10e16 Contents lists available at SciVerse ScienceDirect Journal of Arid Environments journal homepage: www.elsevier.com/locate/jaridenv Effects of seed beetles on the performance of desert legumes depend on host species, plant stage, and beetle density C.W. Fox a,*, W.G. Wallin a, M.L. Bush a, M.E. Czesak b, F.J. Messina c a Department of Entomology, University of Kentucky, S225 Ag Science Center North, Lexington, KY 40546-0091, USA b Biology Department, Vassar College, Poughkeepsie, NY 12604, USA c Department of Biology, Utah State University, Logan, UT 82322-5305, USA article info abstract Article history: Seeds of many arid habitat plants have a water-impermeable coat and can germinate only after being Received 23 May 2011 scarified. Bruchine seed beetles are important parasites of legume seeds in these environments, but their Received in revised form effect on germination can be unpredictable. Beetles deplete seed resources and can kill the embryo but 1 December 2011 also scarify seeds. We investigated the effects of a generalist parasite, Stator limbatus, on the germination Accepted 19 December 2011 and growth of two common legumes in the Sonoran desert, catclaw acacia (Acacia greggii) and blue Available online 9 January 2012 paloverde (Parkinsonia florida). Feeding damage from a single larva greatly increased germination of paloverde but not acacia. This benefit was reduced if seeds were attacked by multiple larvae. Beetle- Keywords: Acacia damaged seeds of both hosts germinated more quickly than did control seeds. Infestation by beetles Germination reduced seedling size, though effects were greater for paloverde than for acacia. Our results demonstrate Paloverde that the effect of S. limbatus can be highly host-specific. In addition, beetle infestation may enhance or Scarification reduce seedling recruitment, depending on the availability of other scarifying agents and the number of Seed parasite larvae per seed. Such contingencies make it difficult to predict the net effect of seed beetles on efforts to Seedling growth control invasive legume hosts or establish native hosts during aridland restoration. Ó 2011 Elsevier Ltd. All rights reserved. 1. Introduction (scarification) that allows water imbibition. Seeds of many arid habitat plants have evolved in association with a variety of scari- Seed germination is influenced by many abiotic and biotic fying agents, including fire, floods, soil abrasion, and soil microor- factors, including rainfall, temperature, soil properties, leaf litter, ganisms (Bewley and Black, 1994). Germination and seedling burial depth, and vegetative cover (Bewley and Black, 1994). The recruitment may also be improved by ingestion and defecation of timing of germination can have profound effects on seedling seeds by mammals and birds (Miller, 1994a; Rohner and Ward, survival and later life-history traits in plants (Kalisz, 1986). Deter- 1999; Traveset et al., 2001). Finally, scarification can be mediated mining the factors that affect germination and early seedling by insect damage, which often produces holes in the seed testa growth is thus necessary to predict the establishment and regen- (Mucunguzi, 1995; Takakura, 2002). eration of plants in native habitats and for choosing appropriate Seed beetles (Coleoptera: Chrysomelidae: Bruchinae) are espe- plants to restore degraded lands (Sy et al., 2001). Many desert cially common predators and parasites of legume seeds in desert legumes play an important role in restoration ecology because they and tropical environments, and many are highly host-specific can tolerate aridity, fix atmospheric nitrogen, and provide food, (Ramirez and Traveset, 2010). Females generally lay eggs on or microhabitats, and shade for a diversity of organisms (Barnes, inside fruits, or they glue their eggs directly to seeds that are 2001; Camargo-Ricalde et al., 2004; Rohner and Ward, 1999). exposed in dehiscent pods or are found on the soil surface In arid and semi-arid environments, germination and seedling (Southgate, 1979). Larvae typically bore into the seed and complete growth are often limited by water availability (Bowers et al., 2004). development within a single seed. In some cases, seed-beetle larvae Many arid habitat legumes produce seeds with an impermeable may attack a majority of seeds in the local plant population, but coat, so that seeds can germinate only after damage to the seed coat infestation rates of some hosts can be chronically low (Miller, 1994a; Takakura, 2002). The net effects of seed beetle infestation on the germination and * Corresponding author. Tel.: þ1 859 257 7474; fax: þ1 859 323 1120. recruitment of host legumes can be unpredictable (Southgate, E-mail address: [email protected] (C.W. Fox). 1979). In some cases, the insect clearly acts as a seed predator; 0140-1963/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.jaridenv.2011.12.008 C.W. Fox et al. / Journal of Arid Environments 80 (2012) 10e16 11 larval feeding effectively kills the embryo or removes so much insect (Fox et al., 2010), we experimentally infested each host endosperm that the seed cannot germinate (Camargo-Ricalde et al., population with the same source population of S. limbatus.A 2004; El Atta, 1993; Tomaz et al., 2007). Larval feeding may also laboratory population of S. limbatus was established >300 beetles create openings for pathogenic bacteria and fungi (Chang et al., that had been collected from >20 A. greggii trees at the Oracle site. 2011; Cipollini and Stiles, 1991; Mucunguzi, 1995). Even if germi- Female S. limbatus oviposit directly onto host seeds inside fruits nation occurs, prior infestation of seeds may distort the develop- that have dehisced or have been damaged by other organisms, such ment of cotyledons or prevent the formation of true leaves (Hegazy as mice or other insects (including other seed beetles, Mitchell, and Eesa, 1991). Depletion of cotyledon reserves may slow plant 1977). Hatching larvae burrow into the seed beneath the oviposi- growth and hence reduce the probability of establishment. Beetle tion site. Because larvae cannot move between seeds, we could damage may even negatively affect non-infested seeds developing control larval density by manipulating the initial number of eggs in the same pods as infested ones, e.g., by mediating allocation of per seed. resource among seeds within the fruit (De Menezes et al., 2010). Despite these detrimental effects of seed-beetle damage, some 2.2. Treatments proportion of infested seeds will germinate successfully in most host populations (Halevy, 1974; Hoffman et al., 1989; Mack 1998; Seeds from each source population were divided among three Miller, 1994b,c). The fate of a damaged seed often depends on its treatments: control (no manipulation), beetle damage, or scarifi- size relative to that of its parasite, as well as the number of larvae cation. We scarified seeds by removing about 5% of the seed coat per seed (Fox et al., 2010). If beetle damage acts as a scarifying with sandpaper, which should promote imbibition of water agent, it can have a large, positive effect on the frequency of without affecting the underlying cotyledons. This technique has germination (Arévalo et al., 2010; Mucunguzi, 1995; Nakai et al., been widely used for physical scarification of desert legume seeds 2011). In one study, beetle infestation was considered a prerequi- (e.g., Patane and Gresta, 2006). To produce beetle-damaged seeds, site to successful germination (Takakura, 2002). Because their mated pairs of beetles were individually confined with five pre- effects on host performance can be so variable, bruchine beetles weighed seeds in a 30-mm Petri dish. Providing only five seeds have been implicated in aiding the spread of undesirable, invasive per dish caused females to lay multiple eggs per seed. Females were legumes (Arévalo et al., 2010) and, conversely, have been proposed allowed to lay eggs for w72 h and discarded. Eggs were scraped as biological control agents for such invasive hosts (van Klinken and from seeds to create densities ranging from one to five eggs per Flack, 2008). seed. Larvae within seeds were reared to adult emergence in This study examines the effects of seed beetle infestation and a laboratory growth chamber at 30 C. Because nearly all eggs hatch damage on two desert legumes: catclaw acacia, Acacia greggii Gray successfully (>95% of eggs hatch; Fox et al., 2007), the number of (Fabaceae: Mimosoideae), and blue paloverde, Parkinsonia florida eggs on a seed is a good estimate of larval density. Seeds from the (Bentham ex A. Gray) S. Watson (Fabaceae: Caesalpinioideae). Both three treatments were randomly interspersed in the chamber to species are common in the southwestern United States and ensure that all seeds experienced similar environmental northwestern Mexico. Germination of acacia and paloverde seeds is conditions. likely to be enhanced by scarification, which in Arizona may be After adult emergence from seeds had been completed, we accomplished by flash floods in gravelly soils, underground removed beetle frass from seeds by tapping the seed and inserting weathering, or ingestion by mammals (Longland et al., 2001; Or a small brush into beetle exit holes. Seeds were then reweighed to and Ward, 2003). Seeds of A. greggii and P. florida are also estimate the amount of mass removed by beetle infestation. frequently attacked by a generalist seed beetle, Stator limbatus Horn Because larval survival can be fairly low in seeds of blue paloverde (Fox et al., 1995, 1997; Siemens et al., 1992). This insect has a rela- (Fox et al., 1995; Fox and Mousseau, 1996), we carefully noted the tively wide geographic distribution and a broad host range total number of adults emerging from each seed. To remove biases (Stillwell et al., 2007, and references therein), but little is known caused by the presence of dead larvae inside seeds, we estimated about this beetle’s impact on host performance. To determine the beetle effects on plant performance using only those seeds from effect of S.
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